The prevalence of hypogonadism in male patients with type 2 diabetes mellitus and clinically relevant factors
Abstract
Aims: Hypogonadism has been reported at high rates in male patients with type 2 diabetes mellitus (T2DM). However, the origin of male hypogonadism in patients with T2DM is poorly known. The aim of this study was to determine the prevalence of hypogonadism and to investigate the potential impact of certain clinical and biochemical variables on hypogonadism in patients with T2DM.
Methods: The study included a total of 513 consecutive males (aged 30 - 60 years) with T2DM who presented at the endocrinology outpatient clinic. The demographic and clinical characteristics of the patients were recorded. Biochemical parameters, total testosterone (TT), gonadotrophins, prolactin, serum lipids, and hemoglobin A1c (HbA1c) were measured. Correlations between metabolic and clinical conditions and T levels were analyzed.
Results: The mean age of the study population was 45.5±12.6 years. Hypogonadism was present in 122 (23.7%) patients, of which 24 (23.3%) were determined with primary hypogonadism. Compared with participants with normal testosterone, those with hypogonadism had lower estimated glomerular filtration rate (eGFR), and the liver function test results, HbA1c and triglycerides levels, and duration of diabetes were higher. Correlation analyses showed that TT was negatively correlated with body mass index (BMI), waist circumference, age, fasting blood glucose, HbA1c, uric acid and triglycerides, and positively correlated with eGFR and high density lipoprotein cholesterol (HDL-C). Multivariate logistic regression analysis revealed that BMI, age, diabetes course, hypertrglyceridemia, hyperuricemia and eGFR <60 ml/min/1.73 m2 are independent risk factors for hypogonadism in male patients with type 2 diabetes.
Conclusion: The current study results demonstrated that the prevalence of hypogonadism is higher in men with type 2 diabetes than in the general population and age, diabetes duration, BMI, triglycerides and uric elevation are independent risk factors.
Keywords
Ethical Statement
Ethics Committee Approval Information: Approving Committee: Health Sciences University, Dışkapı Yıldırım Beyazıt Training and Research Hospital Clinical Research Ethics Committee Approval Date: 17.05.2021 Decision No: 111/11
Supporting Institution
There is no supporting organization
References
- Boyko EJ, Magliano DJ. IDF Diabetes Atlas. 10th ed. International Diabetes Federation; 2021.
- Mushtaq S, Khan K, Abid S, Umer A, Raza T. Frequency of hypogonadism and erectile dysfunction in type-II diabetic patients. Cureus. 2018;10(5):e2654.
- Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: correlations with bioavailable testosterone and visceral adiposity. Diabetes Care. 2007;30(4):911-917.
- Anupam B, Shivaprasad C, Vijaya S, Sridevi A, Aiswarya Y, Nikhil K. Prevalence of hypogonadism in patients with type 2 diabetes mellitus among the Indian population. Diabetes Metab Syndr. 2020;14(5):1299-1304.
- Al Hayek AA, Khader YS, Jafal S, Khawaja N, Robert AA, Ajlouni K. Prevalence of low testosterone levels in men with type 2 diabetes mellitus: a cross-sectional study. J Family Community Med. 2013;20(3):179-186.
- Bhasin S, Brito JP, Cunningham GR, et al. Testosterone therapy in men with hypogonadism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2018;103(5):1715-1744.
- Dandona P, Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. J Clin Endocrinol Metab. 2011;96(9):2643-2651.
- Grossmann M. Low testosterone in men with type 2 diabetes: significance and treatment. J Clin Endocrinol Metab. 2011;96(8):2341-2353.
- Herrero A, Marcos M, Galindo P, Miralles JM, Corrales JJ. Clinical and biochemical correlates of male hypogonadism in type 2 diabetes. Andrology. 2018;6(1):58-63.
- Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabetic Medicine. 1998;15(7):539-553
- The Expert Committee on the Diagnosis and classification of diabetes mellitus. report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 1999;22(1):5-19.
- Agarwal PK, Singh P, Chowdhury S, et al. A study to evaluate the prevalence of hypogonadism in Indian males with Type-2 diabetes mellitus. Indian J Endocrinol Metab. 2017;21(1):64-70.
- Costanzo PR, Knoblovits P. Male gonadal axis function in patients with type 2 diabetes. Horm Mol Biol Clin Investig. 2016;26(2):129-134.
- Ugwu TE, Ikem RT, Kolawole BA, Ezeani IU. Clinicopathologic assessment of hypogonadism in men with type 2 diabetes mellitus. Indian J Endocr Metab. 2016;20(5):667-673.
- Corona G, Bianchini S, Sforza A, Vignozzi L, Maggi M. Hypogonadism as a possible link between metabolic diseases and erectile dysfunction in aging men. Hormones. 2015;14(4):569-578.
- Shi Z, Araujo AB, Martin S, O’Loughlin P, Wittert GA. Longitudinal changes in testosterone over five years in community-dwelling men. J Clin Endocrinol Metab. 2013;98(8):3289-3297.
- Camacho EM, Huhtaniemi IT, O’Neill TW, et al. Age-associated changes in hypothalamic-pituitary-testicular function in middle-aged and older men are modified by weight change and lifestyle factors: longitudinal results from the European Male Ageing Study. Eur J Endocrinol. 2013;168(3):445-455.
- Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab. 2001;86(2):724-731.
- Song, S.H. and C.A. Hardisty, Early-onset Type 2 diabetes mellitus: an increasing phenomenon of elevated cardiovascular risk. Exp Rev Cardiovasc Ther. 2008;6(3):315- 322.
- Zoungas S, Woodward M, Li Q, et al. ADVANCE Collaborative group. Impact of age, age at diagnosis and duration of diabetes on the risk of macrovascular and microvascular complications and death in type 2 diabetes. Diabetologia. 2014;57(12):2465-2474.
- Nanayakkara N, Ranasinha S, Gadowski A, et al. Age, age at diagnosis and diabetes duration are all associated with vascular complications in type 2 diabetes. J Diabetes Complications. 2018;32(3):279-290.
- Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab. 2004; 89(11):5462- 5468.
- Haghighatpanah M, Nejad ASM, Haghighatpanah M, Thunga G, Mallayasamy S. Factors that correlate with poor glycemic control in type 2 diabetes mellitus patients with complications. Osong Public Health Res Perspect. 2018;9(4):167-174.
- Khattab M, Khader YS, Al-Khawaldeh A, et al. Factors associated with poor glycemic control among patients with type 2 diabetes. J Diabetes Complications. 2010;24(2):84-89.
- Tomar R, Dhindsa S, Chaudhuri A, Mohanty P, Garg R, Dandona P. Contrasting testosterone concentrations in type 1 and type 2 diabetes. Diabetes Care. 2006;29(5):1120 -1122.
- Dimopoulou C, Goulis DG, Corona G, Maggi M. The complex association between metabolic syndrome and male hypogonadism. Metabolism. 2018;86:61-68. doi.org/10.1016/j.metabol.2018.03.024
- Shulman GI. Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. N Engl J Med. 2014;371(12):1131-1141.
- Loves S, Ruinemans-Koerts J, de Boer H. Letrozole once a week normalizes serum testosterone in obesity-related male hypogonadism. Eur J Endocrinol. 2008;158(5):741-747.
- Gautier A, Bonnet F, Dubois S, et al. Associations between visceral adipose tissue, inflammation and sex steroid concentrations in men. Clin Endocrinol. 2013;78(3):373-378.
- Brüning JC, Gautam D, Burks DJ, et al. Role of brain insulin receptor in control of body weight and reproduction. Science. 2000;289(5487):2122-2125.
- Wittert G, Grossmann M. Obesity, type 2 diabetes, and testosterone in ageing men. Rev Endocr Metab Disord. 2022;23(6):1233-1242.
- Langer C, Gansz B, Goepfert C, et al. Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochem Biophys Res Commun. 2002;296(5):1051-1057.
- Hernández-Mijares A, García-Malpartida K, Solá-Izquierdo E, et al. Testosterone levels in males with type 2 diabetes and their relationship with cardiovascular risk factors and cardiovascular disease. J Sex Med. 2010;7(5):1954-1964.
- Cameron MA, Maalouf NM, Adams-Huet B, Moe OW, Sakhaee K. Urine composition in type 2 diabetes: predisposition to uric acid nephrolithiasis. J Am Soc Nephrol. 2006;17(5):1422-1428.
- Zong J, Sun Y, Zhang Y, et al. Correlation between serum uric acid level and central body fat distribution in patients with type 2 diabetes. Diabetes Metab Syndr Obes. 2020;13:2521-2531. doi: 10.2147/DMSO.S260891
- Hussain A, Latiwesh OB, Ali F, Younis MYG, Alammari JA. Effects of body mass index, glycemic control, and hypoglycemic drugs on serum uric acid levels in type 2 diabetic patients. Cureus. 2018;10(8):e3158.
Abstract
References
- Boyko EJ, Magliano DJ. IDF Diabetes Atlas. 10th ed. International Diabetes Federation; 2021.
- Mushtaq S, Khan K, Abid S, Umer A, Raza T. Frequency of hypogonadism and erectile dysfunction in type-II diabetic patients. Cureus. 2018;10(5):e2654.
- Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: correlations with bioavailable testosterone and visceral adiposity. Diabetes Care. 2007;30(4):911-917.
- Anupam B, Shivaprasad C, Vijaya S, Sridevi A, Aiswarya Y, Nikhil K. Prevalence of hypogonadism in patients with type 2 diabetes mellitus among the Indian population. Diabetes Metab Syndr. 2020;14(5):1299-1304.
- Al Hayek AA, Khader YS, Jafal S, Khawaja N, Robert AA, Ajlouni K. Prevalence of low testosterone levels in men with type 2 diabetes mellitus: a cross-sectional study. J Family Community Med. 2013;20(3):179-186.
- Bhasin S, Brito JP, Cunningham GR, et al. Testosterone therapy in men with hypogonadism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2018;103(5):1715-1744.
- Dandona P, Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. J Clin Endocrinol Metab. 2011;96(9):2643-2651.
- Grossmann M. Low testosterone in men with type 2 diabetes: significance and treatment. J Clin Endocrinol Metab. 2011;96(8):2341-2353.
- Herrero A, Marcos M, Galindo P, Miralles JM, Corrales JJ. Clinical and biochemical correlates of male hypogonadism in type 2 diabetes. Andrology. 2018;6(1):58-63.
- Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabetic Medicine. 1998;15(7):539-553
- The Expert Committee on the Diagnosis and classification of diabetes mellitus. report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 1999;22(1):5-19.
- Agarwal PK, Singh P, Chowdhury S, et al. A study to evaluate the prevalence of hypogonadism in Indian males with Type-2 diabetes mellitus. Indian J Endocrinol Metab. 2017;21(1):64-70.
- Costanzo PR, Knoblovits P. Male gonadal axis function in patients with type 2 diabetes. Horm Mol Biol Clin Investig. 2016;26(2):129-134.
- Ugwu TE, Ikem RT, Kolawole BA, Ezeani IU. Clinicopathologic assessment of hypogonadism in men with type 2 diabetes mellitus. Indian J Endocr Metab. 2016;20(5):667-673.
- Corona G, Bianchini S, Sforza A, Vignozzi L, Maggi M. Hypogonadism as a possible link between metabolic diseases and erectile dysfunction in aging men. Hormones. 2015;14(4):569-578.
- Shi Z, Araujo AB, Martin S, O’Loughlin P, Wittert GA. Longitudinal changes in testosterone over five years in community-dwelling men. J Clin Endocrinol Metab. 2013;98(8):3289-3297.
- Camacho EM, Huhtaniemi IT, O’Neill TW, et al. Age-associated changes in hypothalamic-pituitary-testicular function in middle-aged and older men are modified by weight change and lifestyle factors: longitudinal results from the European Male Ageing Study. Eur J Endocrinol. 2013;168(3):445-455.
- Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab. 2001;86(2):724-731.
- Song, S.H. and C.A. Hardisty, Early-onset Type 2 diabetes mellitus: an increasing phenomenon of elevated cardiovascular risk. Exp Rev Cardiovasc Ther. 2008;6(3):315- 322.
- Zoungas S, Woodward M, Li Q, et al. ADVANCE Collaborative group. Impact of age, age at diagnosis and duration of diabetes on the risk of macrovascular and microvascular complications and death in type 2 diabetes. Diabetologia. 2014;57(12):2465-2474.
- Nanayakkara N, Ranasinha S, Gadowski A, et al. Age, age at diagnosis and diabetes duration are all associated with vascular complications in type 2 diabetes. J Diabetes Complications. 2018;32(3):279-290.
- Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab. 2004; 89(11):5462- 5468.
- Haghighatpanah M, Nejad ASM, Haghighatpanah M, Thunga G, Mallayasamy S. Factors that correlate with poor glycemic control in type 2 diabetes mellitus patients with complications. Osong Public Health Res Perspect. 2018;9(4):167-174.
- Khattab M, Khader YS, Al-Khawaldeh A, et al. Factors associated with poor glycemic control among patients with type 2 diabetes. J Diabetes Complications. 2010;24(2):84-89.
- Tomar R, Dhindsa S, Chaudhuri A, Mohanty P, Garg R, Dandona P. Contrasting testosterone concentrations in type 1 and type 2 diabetes. Diabetes Care. 2006;29(5):1120 -1122.
- Dimopoulou C, Goulis DG, Corona G, Maggi M. The complex association between metabolic syndrome and male hypogonadism. Metabolism. 2018;86:61-68. doi.org/10.1016/j.metabol.2018.03.024
- Shulman GI. Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. N Engl J Med. 2014;371(12):1131-1141.
- Loves S, Ruinemans-Koerts J, de Boer H. Letrozole once a week normalizes serum testosterone in obesity-related male hypogonadism. Eur J Endocrinol. 2008;158(5):741-747.
- Gautier A, Bonnet F, Dubois S, et al. Associations between visceral adipose tissue, inflammation and sex steroid concentrations in men. Clin Endocrinol. 2013;78(3):373-378.
- Brüning JC, Gautam D, Burks DJ, et al. Role of brain insulin receptor in control of body weight and reproduction. Science. 2000;289(5487):2122-2125.
- Wittert G, Grossmann M. Obesity, type 2 diabetes, and testosterone in ageing men. Rev Endocr Metab Disord. 2022;23(6):1233-1242.
- Langer C, Gansz B, Goepfert C, et al. Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochem Biophys Res Commun. 2002;296(5):1051-1057.
- Hernández-Mijares A, García-Malpartida K, Solá-Izquierdo E, et al. Testosterone levels in males with type 2 diabetes and their relationship with cardiovascular risk factors and cardiovascular disease. J Sex Med. 2010;7(5):1954-1964.
- Cameron MA, Maalouf NM, Adams-Huet B, Moe OW, Sakhaee K. Urine composition in type 2 diabetes: predisposition to uric acid nephrolithiasis. J Am Soc Nephrol. 2006;17(5):1422-1428.
- Zong J, Sun Y, Zhang Y, et al. Correlation between serum uric acid level and central body fat distribution in patients with type 2 diabetes. Diabetes Metab Syndr Obes. 2020;13:2521-2531. doi: 10.2147/DMSO.S260891
- Hussain A, Latiwesh OB, Ali F, Younis MYG, Alammari JA. Effects of body mass index, glycemic control, and hypoglycemic drugs on serum uric acid levels in type 2 diabetic patients. Cureus. 2018;10(8):e3158.
Details
| Primary Language | English |
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| Subjects | Endocrinology |
| Journal Section | Original Article |
| Authors | |
| Early Pub Date | January 7, 2024 |
| Publication Date | January 15, 2024 |
| Submission Date | November 8, 2023 |
| Acceptance Date | December 3, 2023 |
| Published in Issue | Year 2024 Volume: 7 Issue: 1 |
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